Phage particles harboring antibiotic resistance genes in fresh-cut vegetables and agricultural soil

Larrañaga, Olatz; Brown-Jaque, Maryury; Quirós, Pablo; Gómez-Gómez, Clara; Blanch, Anicet R.; Rodríguez-Rubio, Lorena; Muniesa, Maite

doi:10.1016/j.envint.2018.03.019

Cited by 86 publications

(50 citation statements)

References 65 publications

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“…The occurrence of HGT of ARGs was already detected and characterized in clinical environments [33], in wastewater treatment plants (activated sludge) [34,35] and in fertilized soil [36], but still little is known about aquatic environments, especially in open ocean regions. The presence of ARGs in phages and its potential HGT was described in many studies, for example, in a mediterranean river [37], in pig feces samples [38], in fresh-cut vegetables and in agricultural soil [39]. The environmental ARGs sequences found in this study were used as reference for mapping reads from 293 TARA oceans metagenomic samples, in order to quantify each of them around the world.…”

Section: Discussionmentioning

confidence: 88%

Global ocean resistome revealed: exploring Antibiotic Resistance Genes (ARGs) abundance and distribution on TARA oceans samples through machine learning tools

Cuadrat

Sorokina

Andrade

et al. 2019

Preprint

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The rise of antibiotic resistance (AR) in clinical settings is one of the biggest modern global public health concerns, therefore, the understanding of its mechanisms, evolution and global distribution is a priority due to its impact on the treatment course and patient survivability. Besides all efforts in the elucidation of AR mechanisms in clinical strains, little is known about its prevalence and evolution in environmental uncultivable microorganisms. In this study, 293 metagenomic and 10 metatranscriptomic samples from the TARA oceans project were used to detect and quantify environmental Antibiotic Resistance Genes (ARGs) using modern machine learning tools. After extensive manual curation, we show their global distribution, abundance, taxonomy and phylogeny, their potential to be horizontally transferred by plasmids or viruses and their correlation with environmental and geographical parameters. After manual curation, we identified a total of 99,205 environmental ORFs as potential ARGs. These ORFs belong to 560 ARG families that confer resistance to 26 antibiotic classes. A total of 149 ORFs were classified as viral sequences. In addition, 24,567 ORFs were found in contigs classified as plasmidial sequences, suggesting the importance of mobile genetic elements in the dynamics of ARGs transmission. From the 13,163 identified ARGs passing all the criteria for quantification analysis, 4,224 were expressed in at least one of the 10 metatranscriptomic samples (FPKM >5). Moreover, 4,804 contigs with more than 2 ARGs were found, including 2 plasmids with 5 different ARGs, highlighting the potential presence of multi-resistant microorganisms in natural environment and/or non-impacted by human presence oceans, together with the possibility of Horizontal Gene Transfer (HGT) between clinical and natural environments. The abundance of ARGs in 293 samples showed different patterns of distribution, with some classes being significatively more abundant in Coastal Biomes. Finally, we identified ARGs conferring resistance to some of the most relevant clinical antibiotics, revealing the presence of 15 ARGs from the recently discovered MCR-1 family with high abundance on Polar Biomes. A total of 5 MCR-1 ORFs are present in the genus Psychrobacter, an opportunistic bacteria that can cause fatal infections in humans.Our results are available on Zenodo in MySQL database dump format and all the code used for the analyses, including jupyter notebooks can be accessed on github (https://github.com/rcuadrat/ocean_resistome).Recently the number of metagenomic projects stored in public databases have been growing, but the lack of related metadata makes it difficult to conduct highthroughput gene screenings and correlations with environmental factors. Fortunately,

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Section: Discussionmentioning

confidence: 88%

Global ocean resistome revealed: exploring Antibiotic Resistance Genes (ARGs) abundance and distribution on TARA oceans samples through machine learning tools

Cuadrat

Sorokina

Andrade

et al. 2019

Preprint

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“…Although HGT mediated by infectious phages and GTAs have been well studied in vitro, their occurrence in natural environments remains to be fully elucidated (Balcázar, 2018;Grüll et al, 2018). Metagenomic or qPCR-based studies investigating the content of phages/GTAs purified from natural environments impacted by human activities, animal/Human feces, or WWTP sludge and effluents have shown that both particles often carried ARGs (Muniesa et al, 2013;Calero-Cáceres et al, 2014;Ross and Topp, 2015;Colombo et al, 2016;Lekunberri et al, 2017;Brown-Jaque et al, 2018;Larrañaga et al, 2018;Wang et al, 2018). A recent work based on database mining has shown that phage genomes rarely encode ARGs by themselves, therefore suggesting that most phages/GTAs associated ARGs are on transduced bacterial DNA fragments (Enault et al, 2017).…”

Section: Bacteriophage-assisted Dna Transfermentioning

confidence: 99%

Cell-Free DNA: An Underestimated Source of Antibiotic Resistance Gene Dissemination at the Interface Between Human Activities and Downstream Environments in the Context of Wastewater Reuse

2020

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“…For example, only a subset cyano phage capsids deliver their content, and when they do, multiple barriers exist to prevent the recombination of the incoming exogenous DNA in the recipient cell [13], [14], [63] . Future directions to advance our understanding of transduction in the marine environment will involve the direct measurement of host DNA encapsidation in environmental samples [64]- [66] , or if ways to prepare cyanophage capsids loaded with known and traceable DNA are developed, the direct analysis of transduction events [16] .…”

Section: Synthesismentioning

confidence: 99%

Frequency of mispackaging ofProchlorococcusDNA by cyanophage

Raho

Laurenceau

Forget

et al. 2020

Preprint

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Prochlorococcus cells are the numerically dominant phototrophs in the open ocean. Cyanophages that infect them are thus a notable fraction of the total viral population in the euphotic zone, and, as vehicles of horizontal gene transfer, appear to drive their evolution. Here we examine the propensity of three cyanophages -a podovirus, a siphovirus, and a myovirus -to mispackage host DNA in their capsids while infecting Prochlorococcus , the first step in phage-mediated horizontal gene transfer. We find the mispackaging frequencies are distinctly different among the three phages. Myoviruses mispackage host DNA at low and stable frequencies, while podo-and siphoviruses vary in their mispackaging frequencies by orders of magnitude depending on growth light intensity. We attribute this difference to the concentration of intracellular reactive oxygen species and protein synthesis rates. Based on our findings, we propose a model of mispackaging frequency determined by the imbalance between the production of capsids and the number of phage genome copies during infection. RESULTS AND DISCUSSIONHost DNA mispackaging frequency in cyanophage capsids. Using six different loci on the Prochlorococcus MED4 chromosome (representative of the entire chromosome, see Table 3), we quantified the level of mispackaging of MED4 DNA in the capsids of the three different cyanophages (Fig. 1A, Table 2) during infection (Fig. 1B, C). The packaging strategy of the podovirus is T7-like [26] , the myovirus' is likely T4-like headful packaging [27] while the siphovirus' is unknown, but 490 bp direct terminal repeats suggest a T7-like packaging mechanism [28] . Host DNA was detected in the capsids of all 3 cyanophages (Fig. 1C). The levels of mispackaging are low compared to those reported for high transducing phages in S. aureus [29] for example, but comparable to levels (~10 PPM) reported for the marine Synechococcus cyanophage S-PM2 [30] . Corresponding gene Putative functionPrimer sequences (forward and reverse, 5'-3')

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Phage particles harboring antibiotic resistance genes in fresh-cut vegetables and agricultural soil

Cited by 86 publications

References 65 publications

Global ocean resistome revealed: exploring Antibiotic Resistance Genes (ARGs) abundance and distribution on TARA oceans samples through machine learning tools

Global ocean resistome revealed: exploring Antibiotic Resistance Genes (ARGs) abundance and distribution on TARA oceans samples through machine learning tools

Cell-Free DNA: An Underestimated Source of Antibiotic Resistance Gene Dissemination at the Interface Between Human Activities and Downstream Environments in the Context of Wastewater Reuse

Frequency of mispackaging ofProchlorococcusDNA by cyanophage

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